Skip to main content Accessibility help
×
Home

Review: Animal model and the current understanding of molecule dynamics of adipogenesis

  • C. F. Campos (a1) (a2) (a3), M. S. Duarte (a1) (a3), S. E. F. Guimarães (a1) (a3), L. L. Verardo (a1) (a3), S. Wei (a4), M. Du (a2), Z. Jiang (a2), W. G. Bergen (a5), G. J. Hausman (a6), M. Fernyhough-Culver (a7), E. Albrecht (a8) and M. V. Dodson (a2)...

Abstract

Among several potential animal models that can be used for adipogenic studies, Wagyu cattle is the one that presents unique molecular mechanisms underlying the deposit of substantial amounts of intramuscular fat. As such, this review is focused on current knowledge of such mechanisms related to adipose tissue deposition using Wagyu cattle as model. So abundant is the lipid accumulation in the skeletal muscles of these animals that in many cases, the muscle cross-sectional area appears more white (adipose tissue) than red (muscle fibers). This enhanced marbling accumulation is morphologically similar to that seen in numerous skeletal muscle dysfunctions, disease states and myopathies; this might indicate cross-similar mechanisms between such dysfunctions and fat deposition in Wagyu breed. Animal models can be used not only for a better understanding of fat deposition in livestock, but also as models to an increased comprehension on molecular mechanisms behind human conditions. This revision underlies some of the complex molecular processes of fat deposition in animals.

Copyright

Corresponding author

References

Hide All
Aguiari, P, Leo, S, Zavan, B, Vindigni, V, Rimessi, A, Bianchi, K, Franzin, C, Cortivo, R, Rossato, M, Vettor, R, Abatangelo, G, Pozzan, T, Pinton, P and Rizzuto, R 2008. High glucose induces adipogenic differentiation of muscle-derived stem cells. Proceedings of the National Academy of Sciences of the United States of America 105, 12261231.
Albrecht, E, Gotoh, T, Ebara, JF, Xu, X, Viergutz, T, Nurnberg, G, Maak, S and Wegner, J 2011. Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Science 89, 1320.
Caserta, F, Tchkonia, T, Civelek, VN, Prentki, M, Brown, NF, McGarry, JD, Forse, RA, Corkey, BE, Hamilton, JA and Kirkland, JL 2001. Fat depot origin affects fatty acid handling in cultured rat and human preadipocytes. American Journal of Physiology-Endocrinology and Metabolism 280, E238E247.
Cristancho, AG and Lazar, MA 2011. Forming functional fat: a growing understanding of adipocyte differentiation. Nature Reviews Molecular Cell Biology 12, 722734.
Dodson, MV, Hausman, GJ, Guan, L, Du, M, Rasmussen, TP, Poulos, SP, Mir, P, Bergen, WG, Fernyhough, ME, McFarland, DC, Rhoads, RP, Soret, B, Reecy, JM, Velleman, SG and Jiang, Z 2010a. Lipid metabolism, adipocyte depot physiology and utilization of meat animals as experimental models for metabolic research. International Journal of Biological Sciences 6, 691699.
Dodson, MV, Vierck, JL, Hausman, GJ, Guan, LL, Fernyhough, ME, Poulos, SP, Mir, PS and Jiang, Z 2010b. Examination of adipose depot-specific PPAR moieties. Biochemical and Biophysical Research Communications 394, 241242.
Du, M, Huang, Y, Das, AK, Yang, Q, Duarte, MS, Dodson, MV and Zhu, MJ 2013. Meat Science and Muscle Biology Symposium: manipulating mesenchymal progenitor cell differentiation to optimize performance and carcass value of beef cattle. Journal of Animal Science 91, 14191427.
Du, M, Yin, J and Zhu, MJ 2010. Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle. Meat Science 86, 103109.
Du, M and Zhu, MJ 2010. Cellular signaling pathways regulating adipogenesis and marbling of skeletal muscle. Meat Science 86, 103109.
Duarte, MS, Gionbelli, MP, Paulino, PV, Serao, NV, Nascimento, CS, Botelho, ME, Martins, TS, Filho, SC, Dodson, MV, Guimaraes, SE and Du, M 2014. Maternal overnutrition enhances mRNA expression of adipogenic markers and collagen deposition in skeletal muscle of beef cattle fetuses. Journal of Animal Science 92, 38463854.
Duarte, MS, Paulino, PV, Das, AK, Wei, S, Serao, NV, Fu, X, Harris, SM, Dodson, MV and Du, M 2013. Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle. Journal of Animal Science 91, 29382946.
Duarte, SF, Francischetti, EA, Genelhu, VA, Cabello, PH and Pimentel, MM 2007. LEPR p.Q223R, beta3-AR p.W64R and LEP c.-2548G>A gene variants in obese Brazilian subjects. Genetics and Molecular Research 6, 10351043.
Edelman, SV 1998. Type II diabetes mellitus. Advances in Internal Medicine 43, 449500.
Fehrer, C and Lepperdinger, G 2005. Mesenchymal stem cell aging. Experimental Gerontology 40, 926930.
Fernyhough, ME, Hausman, GJ, Guan, LL, Okine, E, Moore, SS and Dodson, MV 2008. Mature adipocytes may be a source of stem cells for tissue engineering. Biochemical and Biophysical Research Communications 368, 455457.
Fernyhough, ME, Helterline, DL, Vierck, JL, Hausman, GJ, Hill, RA and Dodson, MV 2005. Dedifferentiation of mature adipocytes to form adipofibroblasts: more than just a possibility. Adipocytes 1, 1724.
Fischer, J, Koch, L, Emmerling, C, Vierkotten, J, Peters, T, Bruning, JC and Ruther, U 2009. Inactivation of the Fto gene protects from obesity. Nature 458, 894898.
Fraser, JK, Wulur, I, Alfonso, Z and Hedrick, MH 2006. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends in Biotechnology 24, 150154.
Graugnard, DE, Berger, LL, Faulkner, DB and Loor, JJ 2010. High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. British Journal of Nutrition 103, 953963.
Harper, GS and Pethick, DW 2004. How might marbling begin? Australian Journal of Experimental Agriculture 44, 653662.
Hausman, GJ and Dodson, MV 2012. Stromal vascular cells and adipogenesis: cells within adipose depots regulate adipogenesis. Journal of Genomics 1, 5666.
Hausman, GJ, Dodson, MV, Ajuwon, K, Azain, M, Barnes, KM, Guan, LL, Jiang, Z, Poulos, SP, Sainz, RD, Smith, S, Spurlock, M, Novakofski, J, Fernyhough, ME and Bergen, WG 2009. Board-invited review: the biology and regulation of preadipocytes and adipocytes in meat animals. Journal of Animal Science 87, 12181246.
Hocquette, JF, Gondret, F, Baéza, E, Médale, F, Jurie, C and Pethick, DW 2010. Intramuscular fat content in meat-producing animals: development, genetic and nutritional control, and identification of putative markers. Animal 4, 303319.
Hudson, NJ, Reverter, A, Greenwood, PL, Guo, B, Cafe, LM and Dalrymple, BP 2014. Longitudinal muscle gene expression patterns associated with differential intramuscular fat in cattle. Animal 9, 650659.
Jordan, SD, Kruger, M, Willmes, DM, Redemann, N, Wunderlich, FT, Bronneke, HS, Merkwirth, C, Kashkar, H, Olkkonen, VM, Bottger, T, Braun, T, Seibler, J and Bruning, JC 2011. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nature Cell Biology 13, 434446.
Kokta, TA, Dodson, MV, Gertler, A and Hill, RA 2004. Intercellular signaling between adipose tissue and muscle tissue. Domestic Animal Endocrinology 27, 303331.
Komolka, K, Albrecht, E, Wimmers, K, Michal, JJ and Maak, S 2014. Molecular heterogeneities of adipose depots-potential effects on adipose-muscle cross-talk in humans, mice and farm animals. Journal of Genomics 2, 3144.
Kook, SH, Choi, KC, Son, YO, Lee, KY, Hwang, IH, Lee, HJ, Chang, JS, Choi, IH and Lee, JC 2006. Satellite cells isolated from adult Hanwoo muscle can proliferate and differentiate into myoblasts and adipose-like cells. Molecules and Cells 22, 239245.
Lee, EJ, Lee, HJ, Kamli, MR, Pokharel, S, Bhat, AR, Lee, YH, Choi, BH, Chun, T, Kang, SW, Lee, YS, Kim, JW, Schnabel, RD, Taylor, JF and Choi, I 2012. Depot-specific gene expression profiles during differentiation and transdifferentiation of bovine muscle satellite cells, and differentiation of preadipocytes. Genomics 100, 195202.
Lehnert, SA, Wang, YH, Tan, SH and Reverter, A 2006. Gene expression-based approaches to beef quality research. Animal Production Science 46, 165172.
Majka, SM, Barak, Y and Klemm, DJ 2011. Concise review: adipocyte origins: weighing the possibilities. Stem Cells 29, 10341040.
May, SG, Savell, JW, Lunt, DK, Wilson, JJ, Laurenz, JC and Smith, SB 1994. Evidence for preadipocyte proliferation during culture of subcutaneous and intramuscular adipose tissues from Angus and Wagyu crossbred steers. Journal of Animal Science 72, 31103117.
Muthuraman, P 2014. Effect of coculturing on the myogenic and adipogenic marker gene expression. Applied Biochemistry and Biotechnology 173, 571578.
Oikawa, T, Sanehira, T, Sato, K, Mizoguchi, Y, Yamamoto, H and Baba, M 2000. Genetic parameters for grouth and carcass traits of Japanese Black (Wagyu) cattle. Journal of Animal Science 71, 5964.
Pena, F, Molina, A, Aviles, C, Juarez, M and Horcada, A 2013. Marbling in the longissimus thoracis muscle from lean cattle breeds. Computer image analysis of fresh versus stained meat samples. Meat Science 95, 512519.
Penton, CM, Thomas-Ahner, JM, Johnson, EK, McAllister, C and Montanaro, F 2013. Muscle side population cells from dystrophic or injured muscle adopt a fibro-adipogenic fate. PLoS One 8, e54553.
Pethick, DW, Barendse, W, Hocquette, JF, Thompson, JM and Wang, YH 2007. Regulation of marbling and body composition-growth and development, gene markers and nutritional biochemistry. In Energy and protein metabolism and nutrition (ed. I Ortigues-Marty, N Miraux and W Brand-Williams), pp. 7588. Wageningen Academic Publishers, Wageningen, The Netherlands.
Pethick, DW, D’Souza, DN, Dunshea, FR and Harper, GS 2005. Fat metabolism and regional distribution in ruminants and pigs – influences of genetics and nutrition. Recent Advances in Animal Nutrition in Australia 15, 3945.
Pethick, DW, Harper, GS and Oddy, VH 2004. Growth, development and nutritional manipulation of marbling in cattle: a review. Australian Journal of Experimental Agriculture 44, 705715.
Reecy, JM, Miller, SA and Webster, M 2003. Recent advances that impact skeletal muscle growth and development research. Journal of Animal Scence 81, E1E8.
Romao, JM, Jin, W, Dodson, MV, Hausman, GJ, Moore, SS and Guan, LL 2011. MicroRNA regulation in mammalian adipogenesis. Experimental Biology and Medicine. 236, 9971004.
Ryan, KJ, Daniel, ZC, Craggs, LJ, Parr, T and Brameld, JM 2013. Dose-dependent effects of vitamin D on transdifferentiation of skeletal muscle cells to adipose cells. Journal of Endocrinology 217, 4558.
Sadkowski, T, Ciecierska, A, Majewska, A, Oprzadek, J, Dasiewicz, K, Ollik, M, Wicik, Z and Motyl, T 2014. Transcriptional background of beef marbling-novel genes implicated in intramuscular fat deposition. Meat Science 97, 3241.
Sainz, RD and Hasting, E 2000. Simulation of the development of adipose tissue in beef cattle. In Modelling nutrient utilization in farm animals (ed. JP McNamara, J France and DE Beever), pp. 175182. Cabi, New York, NY, USA.
Scraggs, E, Zanella, R, Wojtowicz, A, Taylor, JF, Gaskins, CT, Reeves, JJ, de Avila, JM and Neibergs, HL 2014. Estimation of inbreeding and effective population size of full-blood Wagyu cattle registered with the American Wagyu Cattle Association. Journal of Animal Breeding and Genetics 131, 310.
Shirouchi, B, Albrecht, E, Nuernberg, G, Maak, S, Olavanh, S, Nakamura, Y, Sato, M, Gotoh, T and Nuernberg, K 2014. Fatty acid profiles and adipogenic gene expression of various fat depots in Japanese Black and Holstein steers. Meat Science 96, 157164.
Singh, NK, Chae, HS, Hwang, IH, Yoo, YM, Ahn, CN, Lee, SH, Lee, HJ, Park, HJ and Chung, HY 2007. Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. Journal of Animal Science 85, 11261135.
Sul, HS 2009. Minireview: Pref-1: role in adipogenesis and mesenchymal cell fate. Molecular Endocrinology 23, 17171725.
Taylor-Jones, JM, McGehee, RE, Rando, TA, Lecka-Czernik, B, Lipschitz, DA and Peterson, CA 2002. Activation of an adipogenic program in adult myoblasts with age. Mechanisms of Ageing and Development 123, 649661.
Teboul, L, Gaillard, D, Staccini, L, Inadera, H, Amri, EZ and Grimaldi, PA 1995. Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells. Journal of Biological Chemistry 270, 2818328187.
Wang, YH, Bower, NI, Reverter, A, Tan, SH, De Jager, N, Wang, R, McWilliam, SM, Cafe, LM, Greenwood, PL and Lehnert, SA 2009. Gene expression patterns during intramuscular fat development in cattle. Journal of Animal Science 87, 119130.
Wang, YH, Byrne, KA, Reverter, A, Harper, GS, Taniguchi, M, McWilliam, SM, Mannen, H, Oyama, K and Lehnert, SA 2005. Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mammalian Genome 16, 201210.
Wei, S, Fu, X, Liang, X, Zhu, M, Jiang, Z, Parish, SM, Dodson, MV, Zan, L and Du, M 2015. Enhanced mitogenesis in stromal vascular cells derived from subcutaneous adipose tissue of Wagyu compared with those of Angus cattle. Journal of Animal Science 93, 10151024.
Wertz, AE, Berger, LL, Walker, PM, Faulkner, DB, McKeith, FK and Rodriguez-Zas, SL 2002. Early-weaning and postweaning nutritional management affect feedlot performance, carcass merit, and the relationship of 12th-rib fat, marbling score, and feed efficiency among Angus and Wagyu heifers. Journal of Animal Science 80, 2837.
Yamada, T, Higuchi, M and Nakanishi, N 2014. Fat depot-specific differences in pref-1 gene expression and adipocyte cellularity between Wagyu and Holstein cattle. Biochemical and Biophysical Research Communications 445, 310313.
Yamada, T, Kawakami, SI and Nakanishi, N 2007. Effects of fattening periods on the expression of adipogenic transcription factors in Wagyu beef cattle. Meat Science 76, 289294.
Yamada, T, Kawakami, SI and Nakanishi, N 2009. Expression of adipogenic transcription factors in adipose tissue of fattening Wagyu and Holstein steers. Meat Science 81, 8692.
Yang, A, Larsen, TW, Powell, VH and Tume, RK 1999. A comparison of fat composition of Japanese and long-term grain-fed Australian steers. Meat Science 51, 19.
Zuk, PA, Zhu, M, Ashjian, P, De Ugarte, DA, Huang, JI, Mizuno, H, Alfonso, ZC, Fraser, JK, Benhaim, P and Hedrick, MH 2002. Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell 13, 42794295.

Keywords

Review: Animal model and the current understanding of molecule dynamics of adipogenesis

  • C. F. Campos (a1) (a2) (a3), M. S. Duarte (a1) (a3), S. E. F. Guimarães (a1) (a3), L. L. Verardo (a1) (a3), S. Wei (a4), M. Du (a2), Z. Jiang (a2), W. G. Bergen (a5), G. J. Hausman (a6), M. Fernyhough-Culver (a7), E. Albrecht (a8) and M. V. Dodson (a2)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed